Department of Neurosurgery, The Second Affiliated Hospital of Harbin Medical University, Harbin, China.
Department of Neurosurgery, Emergency Medicine Center, Zhejiang Provincial People's Hospital, Affiliated to Hangzhou Medical College, Hangzhou, China.
Front Immunol. 2022 Mar 3;13:844778. doi: 10.3389/fimmu.2022.844778. eCollection 2022.
5-Methylcytosine (m5C) methylation is an important RNA modification pattern that can participate in oncogenesis and progression of cancers by affecting RNA stability, expression of oncogenes, and the activity of cancer signaling pathways. Alterations in the expression pattern of long non-coding RNAs (lncRNAs) are potentially correlated with abnormalities in the m5C regulation features of cancers. Our aim was to reveal the mechanisms by which lncRNAs regulated the m5C process, to explore the impact of aberrant regulation of m5C on the biological properties of lower-grade gliomas (LGG), and to optimize current therapeutic. By searching 1017 LGG samples from the Cancer Genome Atlas and Chinese Glioma Genome Atlas, we first clarified the potential impact of m5C regulators on LGG prognosis in this study and used univariate Cox analysis and least absolute shrinkage and selection operator regression to explore clinically meaningful lncRNAs. Consequently, we identified four lncRNAs, including LINC00265, CIRBP-AS1, GDNF-AS1, and ZBTB20-AS4, and established a novel m5C-related lncRNAs signature (m5CrLS) that was effective in predicting prognosis. Notably, mutation rate, WHO class II, IDH mutation, 1p/19q co-deletion and MGMT promoter methylation were increased in the low m5CrLS score group. Patients with increased m5CrLS scores mostly showed activation of tumor malignancy-related pathways, increased immune infiltrating cells, and decreased anti-tumor immune function. Besides, the relatively high expression of immune checkpoints also revealed the immunosuppressed state of patients with high m5CrLS scores. In particular, m5CrLS stratification was sensitive to assess the efficacy of LGG to temozolomide and the responsiveness of immune checkpoint blockade. In conclusion, our results revealed the molecular basis of LGG, provided valuable clues for our understanding of m5C-related lncRNAs, and filled a gap between epigenetics and tumor microenvironment.
5- 甲基胞嘧啶(m5C)甲基化是一种重要的 RNA 修饰模式,可通过影响 RNA 稳定性、癌基因表达和癌症信号通路活性参与癌症的发生和进展。长非编码 RNA(lncRNA)表达模式的改变可能与癌症中 m5C 调节特征的异常相关。我们的目的是揭示 lncRNA 调节 m5C 过程的机制,探讨 m5C 异常调节对低级别胶质瘤(LGG)生物学特性的影响,并优化当前的治疗方法。通过从癌症基因组图谱和中国胶质瘤基因组图谱中搜索 1017 个 LGG 样本,我们首先在本研究中阐明了 m5C 调节剂对 LGG 预后的潜在影响,并使用单变量 Cox 分析和最小绝对收缩和选择算子回归来探索有临床意义的 lncRNA。结果,我们鉴定了包括 LINC00265、CIRBP-AS1、GDNF-AS1 和 ZBTB20-AS4 在内的 4 个 lncRNA,并建立了一种新的 m5C 相关 lncRNA 特征(m5CrLS),可有效预测预后。值得注意的是,低 m5CrLS 评分组的突变率、WHO 分级 II、IDH 突变、1p/19q 共缺失和 MGMT 启动子甲基化增加。m5CrLS 评分增加的患者大多表现出与肿瘤恶性相关通路的激活、免疫浸润细胞增加和抗肿瘤免疫功能下降。此外,较高的免疫检查点表达也揭示了高 m5CrLS 评分患者的免疫抑制状态。特别是,m5CrLS 分层对评估 LGG 对替莫唑胺的疗效和免疫检查点阻断的反应性敏感。总之,我们的研究结果揭示了 LGG 的分子基础,为我们理解 m5C 相关 lncRNA 提供了有价值的线索,并填补了表观遗传学和肿瘤微环境之间的空白。